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Evolution of opsin genes in guppies (Poecilia reticulata) relative to male colour: a window into the genetics of mate choice

Periodic Reporting for period 1 - OPSINEVOL (Evolution of opsin genes in guppies (Poecilia reticulata) relative to male colour: a window into the genetics of mate choice)

Reporting period: 2015-04-15 to 2017-04-14

The spectacular colours displayed by males during courtship often result from sexual selection by female choice. Female visual perception and preferences for colour should therefore play a critical role in the evolution of male colours. In guppies, female preferences change repeatedly across populations, presenting a great opportunity to study the genetic mechanisms behind changes in female preferences and mate choice. an. In order investigate the genetic mechanisms of female’s preference for colour, I initially studied opsins, the visual pigments that mediate vision, to estimate how much they vary in females with a clear preference for colourful males and females that have lost this preference. Then I moved on to investigating the genetic basis of female mate choice decisions beyond the eye, in the brain’s visual lobes. To do this I used a combination of behavioural experiments and genomics to identify the genetics pathways that get activated in the female brain when evaluating the nuptial colours of a male. Specifically, I started by evaluating the total number of opsin genes, their conservation across populations as well as variation in opsin sequence and expression. Next I relied on next-generation sequencing, to study the neuromolecular pathways underlying guppy mate preference response in the main visual areas of the brain – telencephalon and optic tectum – of females evaluating attractive males compared to non-attractive males. Although I did not find major differences in the opsins, suggesting all females perceive colour similarly, I am beginning to determine which genes and pathways are turned on in a guppy female’s brain when evaluating males. For example, I found 12 genes are differentially expressed in the telencephalon between females exposed to attractive and non-attractive males, and 162 in the optic tectum. Some of these genes are associated with and organism’s response to stimulus, steroid hormone activity, synaptic plasticity and social behaviour.  
The results of this work will provide a cohesive, integrative and multi-faceted understanding of the role of opsin variation in this model system of evolution by sexual selection, and will determine the role of opsins and the visual system in driving female mate preferences and male colour evolution. This project will help us understand the genetic underpinnings of key adaptive traits, linking genes to the phenotype and opening up new research agendas. The initial results of this work have been published in Science Advances (in press) and Nature Communications (8:14251 - doi:10.1038/ncomms14251).
"1. Complete characterization of the opsin repertoire in the guppy: I used next-generation Illumina sequencing, already being conducted in my host lab for other research questions to gain a complete picture of all opsin loci that informed the rest of this study. I used existing models of opsin function to infer the effect of the sequence differences I observed on opsin spectral sensitivity.

RESULTS:
- Some of the opsin duplicates previously reported for guppies are not present in the genome and thus are the product of amplification artifacts in previous studies.
- I found no evidence of sequence changes that could affect the opsin sensitivity of guppies from different populations.

2. Investigate opsin regulatory evolution across populations: Until recently, studies on animal perception focused on variation in opsin coding sequence and spectral sensitivity, and how changes in these aspects of the visual system could represent adaptations to different light environments. I relied on Nanostring technology to design opsin expression panels in order to measure opsin expression levels in multiple individuals.

RESULTS:
- I found no evidence for differences in opsin expression associated with difference in female preference for colour.
- I found no evidence of sexual dimorphism in opsin gene expression in guppies.
A manuscript with the results of (1) and (2) is currently under preparation.

3. Neurogenomics of female preference. We set up behavioral experiments to quantify differences in female preference for colourful males in various guppy laboratory lines. Based on the results of this initial test, we then set up to investigate the genes involved in mating decisions in guppy females that prefer colourful males and females without such a preference. To do this we designed an experiment where we exposed females to attractive/colourful males or to unattractive/dull males and used RNAseq to measure gene expression in the visual components of the brain (telencephalon and optic tectum) after they evaluate each type of male. We performed this experiment in guppy lines previously shown to differ in the strength of their preference for colorful males to further understand the mechanisms behind variation in female preferences.

RESULTS:
- We found that different laboratory have dramatic differences in female preferences: while some line have a strong and clear preference for colourful males, others do not show evidence of preferring colourful or dull males.
The manuscript “Female brain size affects the assessment of male attractiveness during mate choice"" reporting the results for these initial tests is currently in press in Science Advances.
- We are currently in the process of analyzing the results for the complete experiment. So far we found 12 genes are differentially expressed in the telencephalon between females exposed to attractive and non-attractive males, and 162 in the optic tectum. Some of these genes are associated with and organism’s response to stimulus, steroid hormone activity, synaptic plasticity and social behaviour.
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By integrating comparative methods with state-of-the-art sequencing techniques in guppies, the work done in the framework of this project will greatly contribute to our understanding of evolutionary biology, the evolution of visual systems and more specifically, genetic basis of mate choice and nuptial colours. The multilevel approach of this project will allow me to elucidate the genetic pathways in the brain that are responsible for mating decision not only contributing to our understanding of the genetics of decision making but also the evolution of behaviour and sexual preferences in nature. This project will greatly contribute to making that important and elusive link between genes, phenotype and sexual and natural selection.
This project’s research will also contribute to sensory biology and the evolution of visual systems. Comparative studies among closely related species and populations are rare in the study of colour vision and female preferences.
Illustrations of male and female guppies (credit: Clara Lacy)